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Temporal Dynamics of Bacterial Communities in a Pilot-Scale Vermireactor Fed with Distilled Grape Marc

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Temporal Dynamics of Bacterial Communities in a Pilot-Scale Vermireactor Fed with Distilled Grape Marc microorganisms Article Temporal Dynamics of Bacterial Communities in a Pilot-Scale Vermireactor Fed with Distilled Grape Marc 1, , 1, 2 3,4 María Gómez-Brandón * y, Manuel Aira y, Natielo Santana , Marcos Pérez-Losada and Jorge Domínguez 1 1 Grupo de Ecoloxía Animal (GEA), Universidade de Vigo, E-36310 Vigo, Spain; [email protected] (M.A.); [email protected] (J.D.) 2 Department of Soil Science, Federal University of Santa Maria, 97119-900 Santa Maria, Rio Grande do Sul, Brazil; [email protected] 3 Computational Biology Institute, Department of Biostatistics and Bioinformatics, Milken Institute School of Public Health, George Washington University, Washington, DC 20052, USA; [email protected] 4 CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal * Correspondence: [email protected] These authors contributed equally to this work. y Received: 18 March 2020; Accepted: 25 April 2020; Published: 28 April 2020 Abstract: Vermicomposting has been found as a profitable approach to dispose of and treat large quantities of raw grape marc. However, less information is available with regard to its efficiency for treating distillery winery byproducts, even though distillation has been widely used as a way to economically valorize grape marc. As such, we sought to characterize the compositional and functional changes in bacterial communities during vermicomposting of distilled grape marc by using 16S rRNA high-throughput sequencing. Samples were collected at the initiation of vermicomposting and at days 14, 21, 28, 35 and 42. There were significant changes (p < 0.0001) in the bacterial community composition of distilled grape marc after 14 days of vermicomposting that were accompanied by twofold increases in bacterial richness and diversity from a taxonomic and phylogenetic perspective. This was followed by significant increases in functional diversity of the bacterial community, including metabolic capacity, lignin and cellulose metabolism, and salicylic acid synthesis. These findings indicate that the most striking compositional and functional bacterial community changes took place during the active phase of the process. They also pinpoint functional attributes that may be related to the potential beneficial effects of distilled grape marc vermicompost when applied on soil and plants. Keywords: winery byproducts; steam distillation; earthworms; microbial communities; vermicompost; 16S rRNA; metagenomics 1. Introduction Grape marc, the major solid byproduct of the winemaking industry, has been used as an additive in animal feeding [1], and as a soil conditioner owing to its high level of organic matter and macronutrients [2–7]. This winery byproduct is also sent to distilleries, to recover ethanol for its further use in the elaboration of alcoholic beverages [8,9], and to cosmetic and pharmaceutical industries [6]. Moreover, grape marc can represent a valuable alternative to replace fossil fuels by means of bioethanol generation through distillation [10]. Altogether, it makes distillation a profitable way to economically valorize grape marc. Microorganisms 2020, 8, 642; doi:10.3390/microorganisms8050642 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 642 2 of 19 Nevertheless, the process of distillation also involves the generation of liquid and solid distillery effluents such as vinasses and distilled grape marc that must be treated, disposed of or reused properly to avoid negative environmental impacts [11]. As in raw grape marc, the low pH and the presence of phytotoxic and antimicrobial compounds make distilled grape marc a troublesome waste stream product, which, if not properly treated, can cause soil acidification, groundwater pollution and oxygen depletion in soil [12]. In this sense, stabilization of distilled grape marc via composting has been explored [12–15]. However, the low pH of distilled grape marc poses challenges for large-scale composting trials because it could inhibit the transition between mesophilic and thermophilic composting phases [13]. Co-composting of distilled grape marc with other organic materials like green waste has been shown as a more effective alternative improving not only the compost quality but also shortening the time required to achieve stabilization [14]. Vermicomposting has also been successfully used to dispose of and treat large quantities of raw grape marc [2–7,16,17]. On the one hand, it may provide a means to neutralize the pH of this winery byproduct, as previously shown by Domínguez et al. [2]. And, on the other hand, vermicomposting has been shown to effectively reduce organic biomass and generate high-quality fertilizer with beneficial effects on soil and plants [18,19]. Nonetheless, there is scarce information about the feasibility of vermicomposting for treating distillery residues [20]. Both raw and distilled grape marc are expected to differ in their autochthonous microbiota likely due to the strong selective pressures exerted by high ethanol concentrations, low pH, low oxygen levels and temperature fluctuations in the microbial composition of raw grape marc throughout the distillation process [21]. Such differences in the initial microbial composition of the starting materials may have important consequences for driving bacterial succession during the vermicomposting process [22]. The temporal shifts in microbial communities during vermicomposting can be seen as an example of heterotrophic ecological succession driven by changes in both the quantity and quality of available organic carbon sources. The early changes in the community composition are mainly represented by bacteria that have recently passed through the earthworm gut and been excreted [23]. These egested materials act as a source of microorganisms and nutrients, and their rapid decomposition will result in the release of labile nutrient pools supporting the growth of copiotrophic bacteria, which are characterized by faster rates of carbon turnover, at the earlier time points. As microbial succession progresses, copiotrophic groups will be replaced by oligotrophic bacteria with a higher substrate utilization efficiency and the ability to metabolize the remaining recalcitrant substrates in the casts during the maturation stage [24]. By using sequencing-based microbiome analyses it has enabled us to enhance the throughput, and phylogenetically group and name a larger number of bacterial taxa in the vermicompost microbiome, as recently described for raw grape marc-derived vermicomposts of the cultivars Albariño [25] and Mencía [7]. Moreover, the application of high-throughput sequencing approaches has also facilitated the identification of bacterial taxa that drive keystone functions that may explain the beneficial effects of vermicomposts when applied to the soil and plants [25,26]. However, it is not known yet if the bacterial communities involved in the various stages of vermicomposting of marcs derived from the distillation process will undergo similar compositional and functional changes as those reported for raw grape marc over the course of the process. Therefore, the aim of the present study was to characterize the taxonomic and functional diversity of the bacterial communities involved in the vermicomposting of distilled grape marc of Vitis vinifera L. cv. Albariño in a pilot-scale vermireactor by means of 16S rRNA high-throughput sequencing. 2. Materials and Methods 2.1. Distilled Grape Marc We chose marc derived from distillation of Vitis vinifera cv. Albariño grapes since this grape variety represents 95% of the annual white grape harvest in northwestern Spain. The distilled grape marc was Microorganisms 2020, 8, 642 3 of 19 kindly supplied by a winery located in Pontevedra (Galicia, NW Spain). It was stored at 4 ◦C until needed and turned and moistened with water during two days prior to the vermicomposting trial. 2.2. Vermicomposting Set-Up and Sampling Design The distilled grape marc was processed in a rectangular metal pilot-scale vermireactor (4 m long 1.5 m wide 1 m high) housed in a greenhouse with no temperature control over × × a period of 42 days. The vermireactor set-up has been previously described by Kolbe et al. [25]. The population density of earthworms (Eisenia andrei) was close to its maximum capacity, having a value of 10,923 1783 individuals m 2 that corresponds to 289 72 mature earthworms m 2 and ± − ± − 10,634 1767 immatures m 2, with a mean biomass of 1704 251 g m 2. The earthworm population ± − ± − density in the present study was 36 times higher when compared to that in Kolbe et al. [25]. As a consequence, the vermicomposting time was shortened by half in the current study and the distilled grape marc was completely processed by the earthworms in 42 days. For the characterization of the molecular and the microbial properties, the distilled grape marc layer (12 cm height) was divided into five sections; five samples (10 g) were taken at random from each section at day 0 (fresh distilled grape marc) and after 14, 21, 28, 35 and 42 days of vermicomposting. Samples were bulked and stored in plastic bags at 80 C until needed. − ◦ 2.3. Microbial Activity Microbial activity was assessed as basal respiration by measuring the rate of evolution of CO2 after 6 h of incubation. The evolved CO2 was trapped in NaOH and then measured by titration with HCl to a phenolphthalein endpoint after adding excess BaCl2 [27]. 2.4. DNA Sequencing and Bioinformatic Analyses DNA was extracted from 0.25 g (fresh weight, fw)
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